Arnaud Le Rouzic

Long-term evolution of transposable elements

Transposable elements are often considered parasitic DNA sequences, able to invade the genome of their host thanks to their self-replicating ability. This colonization process has been extensively studied, both theoretically and experimentally, but their long-term coevolution with the genomes is still poorly understood. In this work, we aim to challenge previous population genetics models by considering features of transposable elements as quantitative, rather than discrete, variables. We also describe more realistic transposable element dynamics by accounting for the variability of the insertion effect, from deleterious to adaptive, as well as mutations leading to a loss of transposition activity and to nonautonomous copies. Individual-based simulations of the behavior of a transposable-element family over several thousand generations show different ways in which active or inactive copies can be maintained for a very long time. Results reveal an unexpected impact of genetic drift on the “junk DNA” content of the genome and strongly question the likelihood of the sustainable long-term stable transposition-selection equilibrium on which numerous previous works were based.

Models of the population genetics of transposable elements

Although transposable elements (TEs) have been found in all organisms in which they have been looked for, the ways in which they invade genomes and populations are still a matter of debate. By extending the classical models of population genetics, several approaches have been developed to account for the dynamics of TEs, especially in Drosophila melanogaster . While the formalism of these models is based on simplifications, they enable us to understand better how TEs invade genomes, as a result of multiple evolutionary forces including duplication, deletion, self-regulation, natural selection and genetic drift. The aim of this paper is to review the assumptions and the predictions of these different models by highlighting the importance of the specific characteristics of both the TEs and the hosts, and the host/TE relationships. Then, perspectives in this domain will be discussed.

Evolution of morphological allometry

Morphological allometry refers to patterns of covariance between body parts resulting from variation in body size. Whether measured during growth (ontogenetic allometry), among individuals at similar developmental stage (static allometry), or among populations or species (evolutionary allometry), allometric relationships are often tight and relatively invariant. Consequently, it has been suggested that allometries have low evolvability and could constrain phenotypic evolution by forcing evolving species along fixed trajectories. Alternatively, allometric relationships may result from natural selection for functional optimization. Despite nearly a century of active research, distinguishing between these alternatives remains difficult, partly due to wide differences in the meaning assigned to the term allometry. In particular, a broad use of the term, encompassing any monotonic relationship between body parts, has become common. This usage breaks the connection to the proportional growth regulation that motivated Huxleys original narrow‐sense use of allometry to refer to power–law relationships between traits. Focusing on the narrow‐sense definition of allometry, we review here evidence for and against the allometry‐as‐a‐constraint hypothesis. Although the low evolvability and the evolutionary invariance of the static allometric slope observed in some studies suggest a possible constraining effect of this parameter on phenotypic evolution, the lack of knowledge about selection on allometry prevents firm conclusions.

Dissection of the Genetic Architecture of Body Weight in Chicken Reveals the Impact of Epistasis on Domestication Traits

In this contribution, we study the genetic mechanisms leading to differences in the observed growth patterns of domesticated White Leghorn chickens and their wild ancestor the red jungle fowl. An epistatic QTL analysis for several body-weight measures from hatch to adulthood confirms earlier findings that polymorphisms at >15 loci contribute to body-weight determination in an F2 intercross between these populations and that many loci are involved in complex genetic interactions. Here, we use a new genetic model to decompose the genetic effects of this multilocus epistatic genetic network. The results show how the functional modeling of genetic effects provides new insights into how genetic interactions in a large set of loci jointly contribute to phenotypic expression. By exploring the functional effects of QTL alleles, we show that some alleles can display temporal shifts in the expression of genetic effects due to their dependencies on the genetic background. Our results demonstrate that the effects of many genes are dependent on genetic interactions with other loci and how their involvement in the domestication process relies on these interactions.

Strong and consistent natural selection associated with armour reduction in sticklebacks

Measuring the strength of natural selection is tremendously important in evolutionary biology, but remains a challenging task. In this work, we analyse the characteristics of selection for a morphological change (lateral‐plate reduction) in the threespine stickleback Gasterosteus aculeatus. Adaptation to freshwater, leading with the reduction or loss of the bony lateral armour, has occurred in parallel on numerous occasions in this species. Completely‐plated and low‐plated sticklebacks were introduced into a pond, and the phenotypic changes were tracked for 20 years. Fish from the last generation were genotyped for the Ectodysplasin‐A (Eda) locus, the major gene involved in armour development. We found a strong fitness advantage for the freshwater‐type fish (on average, 20% fitness advantage for the freshwater morph, and 92% for the freshwater genotype). The trend is best explained by assuming that this fitness advantage is maximum at the beginning of the invasion and decreases with time. Such fitness differences provide a quantifiable example of rapid selection‐driven phenotypic evolution associated with environmental change in a natural population.

How To Perform Meaningful Estimates of Genetic Effects

Although the genotype-phenotype map plays a central role both in Quantitative and Evolutionary Genetics, the formalization of a completely general and satisfactory model of genetic effects, particularly accounting for epistasis, remains a theoretical challenge. Here, we use a two-locus genetic system in simulated populations with epistasis to show the convenience of using a recently developed model, NOIA, to perform estimates of genetic effects and the decomposition of the genetic variance that are orthogonal even under deviations from the Hardy-Weinberg proportions. We develop the theory for how to use this model in interval mapping of quantitative trait loci using Halley-Knott regressions, and we analyze a real data set to illustrate the advantage of using this approach in practice. In this example, we show that departures from the Hardy-Weinberg proportions that are expected by sampling alone substantially alter the orthogonal estimates of genetic effects when other statistical models, like F2 or G2A, are used instead of NOIA. Finally, for the first time from real data, we provide estimates of functional genetic effects as sets of effects of natural allele substitutions in a particular genotype, which enriches the debate on the interpretation of genetic effects as implemented both in functional and in statistical models. We also discuss further implementations leading to a completely general genotype-phenotype map.

How does selfing affect the dynamics of selfish transposable elements

BackgroundMany theoretical models predicting the dynamics of transposable elements (TEs) in genomes, populations, and species have already been proposed. However, most of them only focus on populations of sexual diploid individuals, and TE dynamics in populations partly composed by autogamous individuals remains poorly investigated. To estimate the impact of selfing on TE dynamics, the short- and long-term evolution of TEs was simulated in outcrossing populations with various proportions of selfing individuals.ResultsSelfing has a deep impact on TE dynamics: the higher the selfing rate, the lower the probability of invasion. Already known non-equilibrium dynamics (complete loss, domestication, cyclical invasion of TEs) can all be described whatever the mating system. However, their pattern and their respective frequencies greatly depend on the selfing rate. For instance, in cyclical dynamics resulting from interactions between autonomous and non-autonomous copies, cycles are faster when the selfing rate increases. Interestingly, an abrupt change in the mating system from sexuality to complete asexuality leads to the loss of all the elements over a few hundred generations. In general, for intermediate selfing rates, the transposition activity remains maintained.ConclusionsOur theoretical results evidence that a clear and systematic contrast in TE content according to the mating system is expected, with a smooth transition for intermediate selfing rates. Several parameters impact the TE copy number, and all dynamics described in allogamous populations can be also observed in partly autogamous species. This study thus provides new insights to understand the complex signal from empirical comparison of closely related species with different mating systems.

Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism

A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood–based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available.

Harvest-induced disruptive selection increases variance in fitness-related traits

The form of Darwinian selection has important ecological and management implications. Negative effects of harvesting are often ascribed to size truncation (i.e. strictly directional selection against large individuals) and resultant decrease in trait variability, which depresses capacity to buffer environmental change, hinders evolutionary rebound and ultimately impairs population recovery. However, the exact form of harvest-induced selection is generally unknown and the effects of harvest on trait variability remain unexplored. Here we use unique data from the Windermere (UK) long-term ecological experiment to show in a top predator (pike, Esox lucius) that the fishery does not induce size truncation but disruptive (diversifying) selection, and does not decrease but rather increases variability in pike somatic growth rate and size at age. This result is supported by complementary modelling approaches removing the effects of catch selectivity, selection prior to the catch and environmental variation. Therefore, fishing most likely increased genetic variability for somatic growth in pike and presumably favoured an observed rapid evolutionary rebound after fishery relaxation. Inference about the mechanisms through which harvesting negatively affects population numbers and recovery should systematically be based on a measure of the exact form of selection. From a management perspective, disruptive harvesting necessitates combining a preservation of large individuals with moderate exploitation rates, and thus provides a comprehensive tool for sustainable exploitation of natural resources.

Estimation of Genetic Effects and Genotype-Phenotype Maps

Determining the genetic architecture of complex traits is a necessary step to understand phenotypic changes in natural, experimental and domestic populations. However, this is still a major challenge for modern genetics, since the estimation of genetic effects tends to be complicated by genetic interactions, which lead to changes in the effect of allelic substitutions depending on the genetic background. Recent progress in statistical tools aiming to describe and quantify genetic effects meaningfully improves the efficiency and the availability of genotype-to-phenotype mapping methods. In this contribution, we facilitate the practical use of the recently published ‘NOIA’ quantitative framework by providing an implementation of linear and multilinear regressions, change of reference operation and genotype-to-phenotype mapping in a package (‘noia’) for the software R, and we discuss theoretical and practical benefits evolutionary and quantitative geneticists may find in using proper modeling strategies to quantify the effects of genes.